Alleviation of photosynthetic inhibition in copper-stressed tomatoes through rebalance of ion content by exogenous nitric oxide

Copper (Cu) is an essential element that plays a very important role in plant growth and development. Its accumulation in soil is now considered a serious environmental problem endangering agricultural production and human health. In this study, the influence of exogenous nitric oxide (NO) on photosynthesis, Cu, magnesium (Mg), and iron (Fe) contents was studied in tomato seedlings under Cu stress grown in hydroponic culture. The results showed that the addition of sodium nitroprusside (SNP), a donor of exogenous NO, significantly alleviated photosynthetic inhibition in Cu-stressed tomatoes, including the recovery of photosynthetic pigment content and chlorophyll a fluorescence and the improvement of net photosynthetic rate, stomatal conductance, and transpiration rate. Application of exogenous NO by SNP reduced the excessive accumulation of Cu and recovered Mg and Fe contents in Cu-stressed tomatoes. This positive involvement of exogenous NO in tomato tolerance to Cu stress was further confirmed by addition of 2-(4-carboxyphenyl)-4,4,5,5- tetramethylimidazoline-1-oxyl-3-oxide (cPTIO), a specific NO scavenger, which resulted in further reduction of photosynthesis and more severe disturbance of ion homeostasis in Cu-stressed seedlings. These results indicate that rebalance of ion content was involved in alleviation of photosynthesis inhibition in Cu-stressed tomatoes by exogenous NO.

Alleviation of photosynthetic inhibition in copper-stressed tomatoes through rebalance of ion content by exogenous nitric oxide

Copper (Cu) is an essential element that plays a very important role in plant growth and development. Its accumulation in soil is now considered a serious environmental problem endangering agricultural production and human health. In this study, the influence of exogenous nitric oxide (NO) on photosynthesis, Cu, magnesium (Mg), and iron (Fe) contents was studied in tomato seedlings under Cu stress grown in hydroponic culture. The results showed that the addition of sodium nitroprusside (SNP), a donor of exogenous NO, significantly alleviated photosynthetic inhibition in Cu-stressed tomatoes, including the recovery of photosynthetic pigment content and chlorophyll a fluorescence and the improvement of net photosynthetic rate, stomatal conductance, and transpiration rate. Application of exogenous NO by SNP reduced the excessive accumulation of Cu and recovered Mg and Fe contents in Cu-stressed tomatoes. This positive involvement of exogenous NO in tomato tolerance to Cu stress was further confirmed by addition of 2-(4-carboxyphenyl)-4,4,5,5- tetramethylimidazoline-1-oxyl-3-oxide (cPTIO), a specific NO scavenger, which resulted in further reduction of photosynthesis and more severe disturbance of ion homeostasis in Cu-stressed seedlings. These results indicate that rebalance of ion content was involved in alleviation of photosynthesis inhibition in Cu-stressed tomatoes by exogenous NO.

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  • Alaoui-Sossé B, Genet P, Vinit-Dunand F, Toussaint ML, Epron D, Badot PM (2004). Effect of copper on growth in cucumber plants (Cucumis sativus) and its relationships with carbohydrate accumulation and changes in ion contents. Plant Sci 166: 1213–1218.
  • Ali HEM, Ismail GSM (2014). Tomato fruit quality as influenced by salinity and nitric oxide. Turk J Bot 38: 122–129.
  • Andrés-Colás N, Perea-García A, de Andrés SM, Garcia-Molina A, Dorcey E, Rodríguez-Navarro S, Pérez-Amador MA, Puiga S, Peñarrubia L (2013). Comparison of global responses to mild deficiency and excess copper levels in Arabidopsis seedlings. Metallomics 5: 1234–1246.
  • Beligni MV, Lamattina L (2002). Nitric oxide interferes with plant photo-oxidative stress by detoxifying reactive oxygen species. Plant Cell Environ 25: 737–748.
  • Bharwana SA, Ali S, Farooq MA, Iqbal N, Hameed A, Abbas F, Ahmad MSA (2014). Glycine betaine-induced lead toxicity tolerance related to elevated photosynthesis, antioxidant enzymes suppressed lead uptake and oxidative stress in cotton. Turk J Bot 38: 281–292.
  • Chen Y, Shi J, Tian G, Zheng S, Lin Q (2004). Fe deficiency induces Cu uptake and accumulation in Commelina communis. Plant Sci 166: 1371–1377.
  • Chen Y, Zhou Y, Yin TF, Liu CX, Luo FL (2013). The invasive wetland plant Alternanthera philoxeroides shows a higher tolerance to waterlogging than its native congener Alternanthera sessilis. PLoS ONE 8: e81456.
  • Chen Z, Fujii Y, Yamaji N, Masuda S, Takemoto Y, Kamiya T, Yusuyin Y, Iwasaki K, Kato S, Maeshima M et al. (2013). Mn tolerance in rice is mediated by MTP8.1, a member of the cation diffusion facilitator family. J Exp Bot 64: 4375–4387.
  • Connan S, Stengel DB (2011). Impacts of ambient salinity and copper on brown algae: 1. Interactive effects on photosynthesis, growth, and copper accumulation. Aquat Toxicol 104: 94–107.
  • Correa-Aragunde N, Lombardo C, Lamattina L (2008). Nitric oxide: an active nitrogen molecule that modulates cellulose synthesis in tomato roots. New Phytol 179: 386–396.
  • Cuypers A, Keunen E, Bohler S, Jozefczak M, Opdenakker K, Gielen H, Vercampt H, Bielen A, Schellingen K, Vangronsveld J et al. (2012). Cadmium and copper stress induce a cellular oxidative challenge leading to damage versus signaling. In: Gupta DK, Sandalio LM, editors. Metal Toxicity in Plants: Perception, Signaling and Remediation. Heidelberg, Germany: Springer, pp. 65–90.
  • Gill SS, Hasanuzzaman M, Nahar K, Macovei A, Tuteja N (2013a). Importance of nitric oxide in cadmium stress tolerance in crop plants. Plant Physiol Bioch 63: 254–261.
  • Gill SS, Tajrishi M, Madan M, Tuteja N (2013b). A DESD-box helicase functions in salinity stress tolerance by improving photosynthesis and antioxidant machinery in rice (Oryza sativa L. cv. PB1). Plant Mol Biol 82: 1–22.
  • Graziano M, Lamattina L (2007). Nitric oxide accumulation is required for molecular and physiological responses to iron deficiency in tomato plants. Plant J 52: 949–960.
  • Hirayama T, Van de Bittner GC, Gray LW, Lutsenko S, Chang CJ (2012). Near-infrared fluorescent sensor for in vivo copper imaging in a murine Wilson disease model. P Natl Acad Sci USA 109: 2228–2233.
  • Hong JK, Yun BW, Kang JG, Raja MU, Kwon E, Sorhagen K, Chu C, Wang Y, Loake GJ (2008). Nitric oxide function and signalling in plant disease resistance. J Exp Bot 59: 147–154.
  • Ikan R (1969). Natural Products: A Laboratory Guide. New York, NY, USA: Academic Press.
  • Ikari A, Nakajima K, Taki S, Suketa Y (2002). Up-regulation of Na+- dependent Mg2+ transport by nitric oxide and cyclic GMP pathway in renal epithelial cells. Eur J Pharmacol 451: 133–139.
  • Jhanji S, Setia RC, Kaur N, Kaur P, Setia N (2012). Role of nitric oxide in cadmium-induced stress on growth, photosynthetic components and yield of Brassica napus L. J Environ Biol 33: 1027–1032.
  • Kausar F, Shahbaz M, Ashraf M (2013). Protective role of foliar- applied nitric oxide in Triticum aestivum under saline stress. Turk J Bot 37: 1155–1165.
  • Kazemi N (2012). Effect of exogenous nitric oxide on alleviating nickel-induced oxidative stress in leaves of tomato plants. Int J Agri Science 2: 799–809.
  • Kopyra M, Gwoźdź EA (2003). Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus lutrus. Plant Physiol Bioch 41: 1011–1017.
  • Laspina NV, Groppa MD, Tomaro ML, Benavides MP (2005). Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci 169: 323–330.
  • Mihailovic N, Drazic G (2011). Incomplete alleviation of nickel toxicity in bean by nitric oxide supplementation. Plant Soil Environ 57: 396–401.
  • Mur LAJ, Mandon J, Persijn S, Cristescu SM, Moshkov IE, Novikova GV, Hall MA, Harren FJM, Hebelstrup KH, Gupta KJ (2013). Nitric oxide in plants: an assessment of the current state of knowledge. AoB PLANTS 5: pls052.
  • Parasad MNV, Hagemeyer J, editors (1999). Heavy Metal Stress in Plants: From Molecules to Ecosystems. Berlin, Germany: Springer Verlag Press.
  • Pätsikkä E, Kairavuo M, Šeršen F, Aro EM, Tyystjärvi E (2002). Excess copper predisposes photosystem II to photoinhibition in vivo by outcompeting iron and causing decrease in leaf chlorophyll. Plant Physiol 129: 1359–1367.
  • Procházková D, Haisel D, Wilhelmová N, Pavlíková D, Száková J (2013). Effects of exogenous nitric oxide on photosynthesis. Photosynthetica 51: 483–489.
  • Salt DE, Prince RC, Pickering IJ, Raskin I (1995). Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiol 109: 1427–1433.
  • Seth CS, Remans T, Keunen E, Jozefczak M, Gielen H, Opdenakker K, Weyens N, Vangronsveld J, Cuypers A (2011). Phytoextraction of toxic metals: a central role for glutathione. Plant Cell Environ 35: 334–346.
  • Siddiqui MH, Al-Whaibi MH, Basalah MO (2011). Role of nitric oxide in tolerance of plants to abiotic stress. Protoplasma 248: 447–455.
  • Strain HH, Svec WA (1966). Extraction, separation, estimation and isolation of the chlorophylls. In: Vernon GR, Seely GR, editors. The Chlorophyll. New York, NY, USA: Academic Press, pp. 21–66.
  • Taylor NG (2008). Cellulose biosynthesis and deposition in higher plants. New Phytol 179: 239–252.
  • Thounaojam TC, Panda P, Mazumdar P, Kumar D, Sharma GD, Sahoo L, Panda SK (2012). Excess copper induced oxidative stress and response of antioxidants in rice. Plant Physiol Bioch 53: 33–39.
  • Tran TA, Vassileva V, Petrov P, Popova LP (2013). Cadmium-induced structural disturbances in Pisum sativum leaves are alleviated by nitric oxide. Turk J Bot 37: 698–707.
  • Wang L, Yang F, Wang X, Shi Q, Wei M, Hu X (2010a). Effects of exogenous nitric oxide on growth and transcriptional expression of antioxidant enzyme in tomato seedlings under copper stress. Acta Hortic Sin 37: 47–52.
  • Wang L, Yang L, Yang F, Li X, Song Y, Wang X, Hu X (2010b). Involvements of H2O2 and metallothionein in NO-mediated tomato tolerance to copper toxicity. J Plant Physiol 167: 1298– 1306.
  • Wen JF, Gong M, Liu Y, Hu JL, Deng MH (2013). Effect of hydrogen peroxide on growth and activity of some enzymes involved in proline metabolism of sweet corn seedlings under copper stress. Sci Hortic 164: 366–371.
  • Xiong J, Fu G, Tao LX, Zhu C (2010). Roles of nitric oxide in alleviating heavy metal toxicity in plants. Arch Biochem Biophys 497: 13–20.
  • Yang JL, Li YY, Zhang YJ, Zhang SS, Wu YR, Wu P, Zheng SJ (2008). Cell wall polysaccharides are specifically involved in the exclusion of aluminum from the rice root apex. Plant Physiol 146: 602–611.
  • Yang X, Wang X, Wei M, Hikosaka S, Goto E (2009). Changes in growth and photosynthetic capacity of cucumber seedlings in response to nitrate stress. Braz J Plant Physiol 21: 309–317.
  • Yu CC, Huang KT, Kao CH (2005). Nitric oxide reduces Cu toxicity and Cu-induced NH4+ accumulation in rice leaves. J Plant Physiol 162: 1319–1330.
  • Yu Q, Rengel Z (1999). Micronutrient deficiency influences plant growth and activities of superoxide dismutases in narrow- leafed Lupins. Ann Bot 83: 175–182.